Factors Influencing the Risk and Recovery from Sport-Related Concussion

R.J. Elbin ，Tracey Covassin

1 East Tennessee State University

2 Michigan State University

Sport-related concussion remains a hot topic in the field of sport medicine as recent estimates indicate approximately 1.6 to 3 million concussions occur in sport and recreation every year in the United States[1]. The wide array of symptom presentations and cognitive impairments that occur following a concussion has often times made the diagnosis and management of this injury difficult for sports medicine practitioners. The most recent expert recommendations，based on empirical evidence，suggest that every concussed athlete should be managed individually rather than using the more traditional grading scales and return-to-play guidelines which uses a “one size fits all” approach[2]. It is also recommended that implementing a multi-faceted assessment battery that includes a symptom inventory，balance assessment，and neurocognitive testing is best practice for determining recovery following concussion[3]. The ever-growing use of these assessment tools has revolutionized the detection and management of sport-related concussion for sports medicine professionals，and has also afforded researchers an opportunity to use these tools to identify factors that influence recovery from concussion. This article will provide a comprehensive review of the literature that has identified age，sex，and history of concussion as factors that influence the risk and recovery outcomes from sport-related concussion.

Age Differences and Sport-Related Concussion

In the United States，the age of high school athletes (grade 9 – grade 12) range from approximately 14 to 17 years of age，while collegiate athletes are typically 18 to 23 years of age. Researchers who have studied the incidence rates and recovery outcomes from concussion have used age (i.e.，high school vs. college) as a grouping variable. This research has yielded age-related findings that have important clinical implications on the recovery time following sport-related concussion.

High school athletes have been found to demonstrate a slower neurocognitive and symptom recovery following concussion than collegiate athletes[4-7]. In a hallmark study，F(xiàn)ield et al[6]found high school athletes demonstrated significant memory impairment up to 7 days post-concussion，while memory impairment was only observed for the first 24 hours post-concussion in collegiate athletes. High school athletes also reported more concussion symptoms than college athletes at 24 hours，3 and 5 days post-injury[6].Other researchers have also documented significant declines in memory performance at 4 and 7 days postconcussion in high school athletes when compared to non-injured athlete controls[4]. These findings have been supported by other studies that have reported age-related differences in the recovery time following concussion[8，9].

More recent studies have revealed that high school athletes may take even longer to recover from concussion than the 5 to 7 day time period previously reported[4，6，9]. Iverson and colleagues[8]found that 37% of concussed high school athletes were still presenting cognitive impairment on two or more neurocognitive domains (verbal memory，visual memory，reaction time，processing speed) at 10 days post-concussion. Similarly，McClincy and colleagues[9]found memory impairment up to 14 days post-concussion in a sample of concussed high school and collegiate athletes. These studies suggest that high school athletes may take as long as 14 days to recover from concussion.

In contrast to high school athletes，collegiate athletes have been found to demonstrate a faster neurocognitive recovery from sport-related concussion.An earlier study by Macciocchi and colleagues[10]prospectively examined neurocognitive function in a sample of 183 concussed collegiate athletes and matched controls. These researchers found that the neurocognitive decrements in sustained auditory attention and visuomotor speed observed at 24 hours post-concussion were resolved within 5 days of injury.Other researchers have supported this finding as both McCrea et al[5]and Field et al[6]did not report any neurocognitive impairments past 5 days post-injury in college athletes. These findings suggest that college athletes generally experience a rapid resolution of cognitive impairments following concussion.

In accounting for these age-related differences，researchers have suggested that the immature or developing brain places younger athletes (i.e.，high school) at risk for more adverse outcomes following concussion. Specifically，developmental differences in neck strength and skull size have been suggested to predispose younger athletes to an increased risk for concussion and could also prolong recovery[11，12].Other findings from animal models have reported an increased sensitivity to glutamate-mediated N-methyl-D-aspartate (NMDA) which is a prevalent neurotransmitter released in the brain following concussion[13，16]. This hypersensitivity places the younger athlete at an increased risk for a secondconcussion in the days following injury[17]. Therefore it has been recommended that the high school athlete be managed conservatively to avoid any catastrophic consequences that could result from sustaining another concussion before the first injury completely resolves[17].

These pathophysiological and biomechanical differences between the developing and the adult brains are plausible explanations for the age-related differences in the risk and recovery of concussion.These differences call criticism to traditional concussion management and return-to-play guidelines，as they assume that the speed of recovery is uniform between younger and older athletes[6，7]. Moreover，these guidelines also manage male and female concussed athletes the same. However，researches have also revealed sex differences in the risk for and recovery from sport-related concussion[18-20].

Sex Differences and Sport-Related Concussion

In the United States there has been a steady increase in female sport participation at both the high school and collegiate levels[21，22]. During the 2007-2008 academic year a record setting 3 million females participated in high school athletics[22].All-time highs for female sport participation were also found for collegiate women athletes as 175,994 women athletes participated in sport during the 2007-2008 academic year[21]. This increase in female sport participation has prompted researchers to study sex differences in the prevalence and incidence of sportrelated concussion in both high school and collegiate populations[23-27].

Several researchers have reported sex differences in the incidence of sport-related concussion at both the high school[25，26]and collegiate level[20，23，27].Hootman and colleagues[27]recently summarized 16 years (1988-2004) of NCAA injury data and also found differences in the incidence of concussion between male and female athletes. These researchers also reported that concussion comprised a greater percentage of total injuries in women’s soccer(5.3%)，basketball (4.7%)，and lacrosse (6.3%)when compared to men’s soccer (3.9%)，basketball(3.2%)，and lacrosse (5.6%). Gessel and colleagues[26]found that in high school sports played by both sexes (soccer and basketball)，girls had a higher incidence of concussion than boys. Specifically，girls’soccer (21.5%) and basketball (9.5%) had a higher incident of concussion than boys’ soccer (15.4%) and basketball (2.81%)[26]. These data clearly suggest that sex differences likely exist for the incidence of concussion，with female athletes having a higher incidence of concussion. This increase in the incidence of concussion may be due to increased awareness of the signs and symptoms of concussive injury.

The sex differences in the incidence of sportrelated concussion have also prompted consideration of potential differences in cognitive outcomes and symptom presentation between males and females following this injury. Since males and females differ on cognitive measures of verbal memory[24，28-30],perceptual motor speed[30，31], and visuospatial tasks[24，30，32], researchers have explored the nature of these differences following concussion. This disparity in cognitive performance may contribute to different recovery patterns following concussion[18].Unfortunately empirical work in this area is scant，but the initial findings are promising and warrant further investigation[18，24，33].

Broshek and colleagues[18]administered a computerized neurocognitive test battery to 94 male and 37 female athletes prior to (i.e.，baseline) and approximately 3 to 4 days following concussion.Post-injury sex comparisons on neurocognitive measures indicated that female athletes demonstrated significantly more severe cognitive declines (relative to baseline scores) than males in simple and choice reaction time. Significantly more symptoms were also self-reported by females compared to males following concussion. Moreover，female athletes demonstrated cognitive impairment 1.7 times more often than male athletes in simple and choice reaction time. These findings were among the first to suggest that sex differences may exist following sport-related concussion.

Covassin et al[19]examined sex differences on measures of cognitive performance and self-reported symptoms following sport-related concussion. Similar to Broshek et al[18]，Covassin and colleagues[19]also employed a computerized neurocognitive test battery at baseline and at approximately 2 and 8 days postconcussion to a sample of 79 (41 male； 38 female)concussed collegiate athletes. These authors found an expected decrease in cognitive performance in both male and female athletes at 2 and 8 days following concussion. However，sex differences in one of four cognitive domains were noted，as concussed females performed significantly worse in visual memory than concussed males at 2 days post-concussion.In addition，concussed male athletes reported significantly higher symptom scores for sadness and vomit than females. These findings are inconsistent with previous studies that reported females，not males，to self-report more symptoms following concussion[18，34]. These differing post-injury outcomes between concussed male and female athletes have been attributed to various differences in hormonal systems，cerebral organization，and weaker neck musculature that may inf l uence females’ risk for more adverse outcomes following concussion[18].

The research suggesting there are differences in age (e.g.，high school vs. college) and sex on the risk and recovery from concussion is strong. Findings have been replicated and are becoming generally accepted across the field of sports medicine. Moreover，the varying risks and recovery patterns between male and female high school and collegiate athletes have a direct inf l uence on the management of concussion. However there is still debate on the cumulative effects associated with history of concussion. It is common knowledge that once an athlete gets his or her first concussion，it is likely he or she will sustain future concussions and may even take longer to recover，however the longterm effects from multiple concussions are still unclear.

History of Concussion and Concussion Outcomes

There is vested interest from coaches，parents，and sports medicine professionals to ensure the safety of athletes upon their return to play following concussion. Determining when a concussed athlete can resume sports participation may be a difficult decision when the athlete has a history of previous concussion(s)，due to the growing body of evidence suggesting possible detrimental effects of previously sustained concussions[35]. The question，“How many is too many?” is still a debated topic among sports medicine professionals and researchers. Empirical studies have continued to investigate the assumption that a history of multiple concussions are predictive of a lowered threshold (i.e.，increase in risk) and worse outcome(i.e.，increased symptoms and prolonged cognitive impairments) following subsequent concussion[36].The existing literature on this topic has addressed the influence history of concussion has on the risk for future concussion，recovery from incident concussion，and cognitive performance over time.

Zemper[37]investigated the incidence of sportrelated concussion in both high school and college football players with a history of concussion.Interestingly both high school and college football players with a history of concussion were 5.8 times more likely to sustain a concussion than those without a history of concussion. In addition，high school football players with a history of concussion had a slightly higher risk (6.6 times greater) for subsequent concussion than collegiate football players (5.3 times greater) with a history of concussion. This finding failed to support the authors’ hypothesis that collegiate athletes would be at a higher risk of concussion due to a longer involvement in sport than high school athletes.However，it complements other studies that have found age-related differences on concussion risk and outcomes that are attributed to the on-going cognitive and physical development of high school athletes[6].A “dose-response” relationship between the number of previous concussions and the risk of future concussion has been suggested by researchers[38].Guskiewicz and colleagues[38]conducted a 3-year study that examined the cumulative effects associated with recurrent concussion in a large sample of collegiate football players. These researchers found an association between the reported number of previous concussions and the likelihood of incident concussion.Specifically，athletes with a history of three or more previous concussions were 3.4 times more likely to sustain a concussion than those without a previous history of concussion. Additionally，athletes with two previous concussions were 2.8 times more likely and athletes with only one previous concussion were 1.5 times more likely to sustain a subsequent concussive injury than athletes without a previous history of concussion. These researchers also concluded that 1 in 15 athletes who sustain a concussion may incur another concussion in the same season. Moreover，these re-injuries typically take place within a 7 to 10 day period following concussion[38]. These researchers concluded that college football players with a history of concussion are likely to have future concussive injuries，and support a dose-response effect for the number of previous concussions and subsequent risk of injury.

History of Concussion and Recovery Time from Future Concussion

In addition to the increased risk of future concussion associated with a history of concussion，it also appears that history of concussion predisposes athletes to a more prolonged recovery from future concussive injury. Covassin and colleagues[33]prospectively administered a computerized neurocognitive test battery to a sample of concussed(2 or more concussions vs no previous concussion)collegiate athletes at approximately 2 and 5 days postconcussion. There were no significant differences between groups at 2 days post-concussion，however，at approximately 5 days post-concussion，athletes with a history of two or more concussions demonstrated lower performance on verbal memory and slower reaction times compared to athletes without a history of concussion. These results suggest that athletes with a history of two or more concussions may take longer to recover than athletes with no history of concussion.

Researchers have also examined the cognitive recovery from concussion between athletes with and without a history of three or more concussions[35].Concussed athletes with a history of three or more concussions have been found to demonstrate significant memory impairment at 2 days post-injury compared to concussed athletes without a history of concussion(i.e.，recovering from their first injury). Athletes with a history of multiple concussions were also 7.7 times more likely to demonstrate a major decrease in memory performance than athletes with no previous concussion 2 days post-injury. These results are in agreement with previous literature that found athletes with a history of three or more concussions presented a greater number of post-concussion symptoms[39]and take longer for symptoms to resolve[38]than athletes without a history of concussion.

The aforementioned studies collectively suggest that a dose-response relationship between the number of previous concussions and outcome from subsequent concussion likely exists[35，38]. Therefore athletes with a history of a single concussion are not likely to demonstrate any worse neurocognitive or symptom outcomes following subsequent concussive injury[40].In contrast，athletes who have sustained at least two prior concussions may demonstrate a more prolonged neurocognitive and symptom recovery following incident concussion[33，35]. This research is conclusive in suggesting that the risk and outcome associated with future concussive injury are a likely function of the number of previous concussions. Unfortunately studies investigating more long-term cumulative effects of multiple concussions are less conclusive[35，41-44].

Cumulative Effects of Multiple Concussions

The potential for long lasting，or permanent neurocognitive impairment resulting from multiple concussions are a central concern for athletes，families，coaches，and sports medicine professionals[45]. In addition，the recent media attention from the suggested association between latelife cognitive impairment (e.g.，memory) associated with multiple concussions found in retired professional football players has caused concern for amateur athletes[46]. Consequently，researchers have studied neurocognitive performance in high school[43，47]，collegiate[48，49]， and professional athletes[50，51]with a history of multiple concussions. Unfortunately these studies have produced conf l icting results，leaving this important issue still in debate.

College athletes with a history of multiple concussions have been found to demonstrate poor performance on more formal paper-and-pencil neurocognitive test batteries and increased symptoms[48，49]. Collins et al[48]assessed neurocognitive function and self-reported symptoms in a large sample of college football players. These athletes were separated into three groups (none，one，two or more previous concussions) according to selfreport of concussion history. The results of this study indicated that baseline symptoms increased as the number of previously sustained concussions increased.Other findings revealed that athletes with two or more concussions performed significantly worse than the other two groups on Trail-Making Test B and the Symbol Digit Modalities test. These researchers concluded that history of multiple concussions is associated with long-term deficits in executive function and information processing speed.

Other researchers have failed to find any evidence of impaired cognitive function in collegiate athletes with and without a history of multiple concussions[52].Guskiewicz et al[52]found collegiate soccer players demonstrated similar performance on a battery of neurocognitive tests compared to other collegiate athletes (e.g.，baseball，women’s lacrosse and field hockey) and student controls[52]. In addition，soccer athletes with a history of two or more concussions were no more likely to have impaired neurocognitive performance than soccer athletes with no history of concussion[52]. These findings suggest that there are no cumulative effects associated with multiple concussions.

Very few studies have considered the cumulative effects of multiple concussions in high school athletes，which is surprising due to the increased vulnerability and prolonged recovery times from concussion seen in this younger population[6]. However，the few studies that have been published reveal there may be a cause for concern for these younger athletes，as there is documented evidence that suggests a history of multiple concussions may be associated with decreased neurocognitive function. Moser and colleagues[44]assigned athletes to the following groups： no previous concussion； one previous concussion； two or more previous concussions； and recently concussed(within the past 7 days). These recently concussed athletes performed significantly worse on measures of attention，concentration，processing speed，and cognitive flexibility than those in the no concussion history or one previous concussion groups. Strikingly，there were no statistical differences on any of these measures of cognitive ability between recently concussed athletes and athletes with a history of two or more concussions.

Researchers have thoroughly examined the relationship between history of concussion and the subsequent risk and outcome from future concussive episodes. In sum，athletes with a history of at least two or more concussions have been found to be at a higher risk for subsequent concussion，and are likely to demonstrate a prolonged recovery from future concussive injuries[38，43，44]. However，the extant literature investigating more long-term or residual cognitive impairments associated with a history of multiple concussions has uncovered many issues and left many questions unanswered.

Age，sex，and history of concussion should be considered when assessing and managing concussion in both the sport and recreation setting. The numerous studies that have focused on the inf l uence that each of these individual factors have on concussion risk and recovery emphasize that every concussed athlete is different and should be managed individually. Sports medicine professionals that give consideration to these individual differences among their athletes will be more knowledgeable and better prepared to detect and manage this injury.

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